Life strategy, ecophysiology and ecology of seaweeds in polar waters

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Abstract Polar seaweeds are strongly adapted to the low temperatures of their environment, Ant- arctic species more strongly than Arctic species due to the longer cold water history of the Ant- arctic region. By reason of the strong isolation of the Southern Ocean the Antarctic marine flora is characterized by a high degree of endemism, whereas in the Arctic only few endemic species have been found so far. All polar species are strongly shade adapted and their phenology is finely tuned to the strong seasonal changes of the light conditions. The paper summarises the

present knowledge of seaweeds from both polar regions with regard to the following topics: the history of seaweed research in polar regions; the environment of seaweeds in polar waters; biodiversity, biogeographical relationships and vertical distribution of Arctic and Antarctic seaweeds; life histories and physiological thallus anatomy; temperature demands and geographical distribution;

light demands and depth zonation; the effect of salinity, temperature and desiccation on supra- and eulittoral seaweeds; seasonality of reproduction and the physiological characteristics of

C. Wiencke (&)ÆU. H. Lu¨der

Alfred Wegener Institute for Polar and Marine Research, Am Handelshafen 12, D-27570 Bremerhaven, Germany

e-mail: cwiencke@awi-bremerhaven.de M. N. Clayton

School of Biological Sciences, Monash University, P.O Box 18, Melbourne, Victoria 3800, Australia I. Go´mez

Instituto de Biologı´a Marina, Universidad Austral de Chile, Casilla 567, Valdivia, Chile

K. Iken

Institute of Marine Science, University of Alaska Fairbanks, O’Neill Bldg., Fairbanks, AK 99775, USA C. D. Amsler

Department of Biology, University of Alabama at Birmingham, Birmingham, AL 35294-1170, USA

U. Karsten

Institute of Biological Sciences,

Applied Ecology, University of Rostock, Albert-Einstein-Strasse 3, D-18051 Rostock, Germany

D. Hanelt

Biocenter Klein Flottbek, University

of Hamburg, Ohnhorst-Str. 18, D-22609 Hamburg, Germany

K. Bischof

Institute for Polar Ecology, University of Kiel, Wischhofstr. 1–3, D-24148 Kiel, Germany

K. Dunton

Marine Science Institute, University of Texas at Austin, 750 Channel View Drive, Port Aransas, TX 78373, USA

DOI 10.1007/s11157-006-9106-z R E V I E W

Life strategy, ecophysiology and ecology of seaweeds in polar waters

C. WienckeÆ M. N. ClaytonÆ I. Go´mezÆ K. Iken ÆU. H. Lu¨derÆC. D. AmslerÆ

U. KarstenÆD. HaneltÆ K. BischofÆK. Dunton

Received: 7 March 2006 / Accepted: 8 May 2006 Springer Science+Business Media B.V. 2006

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microscopic developmental stages; seasonal growth and photosynthesis; elemental and nutri- tional contents and chemical and physical defences against herbivory. We present evidence to show that specific characteristics and adapta- tions in polar seaweeds help to explain their ecological success under environmentally extreme conditions. In conclusion, as a perspective and guide for future research we draw attention to many remaining gaps in knowledge.

Keywords Chemical ecologyÆ FreezingÆ Growth ÆLightÆPhenologyÆ PhotosynthesisÆ Polar algaeÆ SalinityÆSeaweedsÆTemperature

History of seaweed research in the polar regions

The first phycological studies in the Arctic and the Antarctic regions took place in the first half of the 19th century. Studies on Antarctic seaweeds started in 1817 with the work of Gaudi- chaud, Bory, Montagne, Hooker and Harvey (Godley 1965). Later, between 1882 and 1909, intensive studies were carried out by Skottsberg, Reinsch, Gain, Hariot, Kylin, Hylmo¨, Foslie and others (Papenfuss 1964). After this period of mostly taxonomic and biogeographical investigations, which culminated in the publication of the catalogue by Papenfuss (1964), numerous diving investigations were conducted in West Antarctica by, among others, Neushul (1965), De´le´pine et al.

(1966), Lamb and Zimmermann (1977), Moe and DeLaca (1976), Richardson (1979), Klo¨ser et al.

(1996) and in East Antarctica by Zaneveld (1968) and Cormaci et al. (1997). These studies gave greater insight into the depth distribution of Antarctic seaweeds and allowed more detailed studies on the life histories, ecophysiology and ecology of seaweeds from Antarctica. The highly fragmented information on the seaweeds of Antarctica was summarized recently in a synopsis by Wiencke and Clayton (2002).

Early algal research in the Arctic started in 1849 in the Canadian Arctic with Harvey and Dickie (Lee 1980). The Russian phycologist Kjellman worked in many places in the Arctic, especially in the Russian Arctic, the northern Bering Sea and Spitsbergen. His book ‘‘The algae

of the Arctic Sea’’ (Kjellman 1883) is a taxonomic and biogeographic baseline study. Detailed studies on seaweeds from Greenland were made by Rosenvinge (1898), and in the 20th century by Lund (1951, 1959a, b) and Pedersen (1976).

Taxonomic information concerning seaweeds from Spitsbergen and the Russian Arctic is also available in publications by Svendsen (1959), Zi- nova (1953; 1955), Vinogradova (1995) and many others. A very valuable contribution on seaweeds from the north-eastern coast of North America is the book by Taylor (1966; first published 1937).

The first extensive diving studies were performed by Wilce (1963), Chapman and Lindley (1980) and by Dunton et al. (1982) in the Canadian and Alaskan Arctic. As in Antarctica, diving is an essential prerequisite for detailed studies on all aspects of seaweed biology and this technique has since been widely applied in several regions of the Arctic. Since 1991 there has been intensive research on the ecology and ecophysiology of Arctic seaweeds on Spitsbergen (Hop et al. 2002;

Wiencke 2004).

The environment of seaweeds in polar waters

The polar regions are characterized by pronounced seasonal variations of the light regime, low temperatures, and long periods of snow and ice cover. Littoral seaweed communities are often strongly impacted by icebergs and sea ice especially in areas with high wave action (Klo¨ser et al.

1994). Icebergs can run aground in the Antarctic down to 600 m depth (Gutt 2001). First-year sea ice has a thickness of up to 2 m, and in the Arctic multi-year ice can reach depths of about 40 m (Gutt 2001). Anchor ice forms on the seabed in shallow waters and can enclose seaweeds especially in East Antarctica (Miller and Pearse 1991).

The seasons in the sublittoral are characterized in polar regions by short periods of favourable light conditions and extended periods of darkness due to the polar night and sea ice cover in winter (Kirst and Wiencke 1995). At the poleward distribution limits of seaweeds, at 77S and 80N, respectively, the annual solar radiation is 30–50% less than in temperate to tropical regions, and the polar night lasts for about 4 months

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(Lu¨ning 1990). At lower latitudes, e.g. close to the northern limit of the Antarctic region, in the South Shetland Islands, daylength varies between 5 h in winter and 20 h in summer (Wiencke 1990a). This extreme light regime has strong implications for primary productivity in general and for the seasonal development of seaweeds. In addition the long periods of darkness are further extended due to the formation of sea ice. If the ice is also covered by snow, irradiance can be diminished to less than 2% of the surface value.

Consequently, seaweeds may be exposed up to about 10 months of darkness or very low light conditions (Chapman and Lindley 1980; Dunton 1990; Miller and Pearse 1991; Drew and Hastings 1992; Klo¨ser et al. 1993).

After sea ice break-up in spring, light pene- trates deeply into the clear water. On King George Island (South Shetland Islands) at this time average photon fluence rates are 70lmol m^–2s^–1 at midday in 30 m depth (Go´mez et al.

1997). On Signy Island (South Orkney Islands) the euphotic zone, i.e. the 1% depth for photosyn- thetically active radiation (PAR), was determined at 29 m (Brouwer 1996). UV-radiation (UVR) and blue light are, however, more strongly attenuated. The 1% depth for UVB radiation, repre- senting more or less the threshold irradiance of UV-B with the potential to affect primary plant productivity negatively, is located between 4 and 8 m on Spitsbergen (Hanelt et al. 2001; van de Poll et al. 2002). Later, in summer, coastal waters in polar regions become more turbid due to the development of phytoplankton blooms and the inflow of melt water carrying fine sediments and detritus that strongly affect light transmission.

With increasing turbidity the wavelengths shift from the blue to the green waveband in deep waters (Jerlov 1976). Consequently, sublittoral seaweeds are exposed only to low irradiances even though the sun altitude is relatively high (e.g.

about 34elevation in July compared to only 14 in April at 79North at noon).

In a canopy of kelps or other overstory brown algae, PAR is strongly attenuated, and understorey species are exposed to even lower irradiances (Hanelt et al. 2003). The light quality also changes.

Below the canopy the spectrum is enriched in green and in far red light, probably affecting photosyn-

thesis as well as the photomorphogenetic development of the understorey (Salles et al. 1996).

The possible impact of enhanced UVB radiation due to stratospheric ozone depletion on primary production of seaweeds is higher during the spring season, as organisms in the eulittoral and upper sublittoral zone are already affected by UVB radiation throughout the polar day and turbid melt water input occurs only during the summer season. The strong increase of turbidity due to a discharge of sediments by melt water and glaciers applies especially to Arctic shorelines in half- open fjord systems where the water exchange with the clearer oceanic water is retarded (Svendsen et al. 2002). On open coastlines the melt water is exchanged much faster with clear oceanic water so that seaweeds are exposed to biologically effective UVR for longer time periods.

The inflow of melt water in summer has considerable effects on the salinity and temperature regime in inshore waters. During times of calm weather, there is a strong stratification in the water body with a layer of fresh water above a layer of denser sea water. However, due to vertical water mixing by wave action and wind the deeper water zones also become affected and a salinity decrease may occur down to about 20 m depth (Hanelt et al. 2001).

In contrast to the strong seasonal variation in the radiation conditions, water temperatures in the sublittoral mostly change only little between – 1.8C in winter and +2.0C in summer, e.g. in the Antarctic Peninsula region (Drew and Hastings 1992; Klo¨ser et al. 1993). At the boundary with the temperate region, maximum summer temperatures can go up to about 5C in the Antarctic and up to about 8–10C in the Arctic (Wiencke and tom Dieck 1989; Lu¨ning 1990; Svendsen et al. 2002).

Macronutrient concentrations are high and not limiting for seaweeds at any time of the year in the Antarctic (Deacon 1937; Drew and Hastings 1992). However, iron concentrations are low in the Antarctic and inhibit phytoplankton growth (de Baar 1994; de Baar et al. 1995). Whether iron deficiency also affects seaweeds is unclear. High macronutrient concentrations are also present in the area of Spitsbergen, which obtains nutrient- rich water from the south during parts of the year (the so-called Spitsbergen current). This is one

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reason why the seas of the European Arctic belong to the most productive seas in the world (Orheim et al. 1995). In general, there is a considerable seasonal fluctuation of macronutrients.

Nitrogen and phosphorus levels are relatively high during the winter months but both macronutrients are almost fully depleted in summer (Chapman and Lindley 1980). This applies also to the area close to Spitsbergen (Aguilera et al.

2002).

The tidal amplitudes on King George Island and on Spitsbergen vary between 120 and 150 cm (Scho¨ne et al. 1998; Svendsen et al. 2002). Like terrestrial vegetation, supra-and eulittoral seaweeds are exposed to strongly changing light conditions and temperatures, but also frequently to desiccation and low or high salinities due to the tidal regime and the weather. Photon fluence rates close to terrestrial cryptogams in the mari- time Antarctic vary between 0.1 mol m^–2 d^–1 in winter and more than 30 mol m^–2d^–1 with max- ima around 1600lmol m^–2s^–1 in summer (Schroeter et al. 1995; Winkler et al. 2000). The annual variation of thallus temperatures of a lichen growing on a coastal rock on King George Island (Antarctica) was between +27.4C in summer and –27.3C in winter (Schroeter et al.

1995). However, smaller annual amplitudes of only 10C also occur depending on the degree of exposure and snow cover (Winkler et al. 2000).

With increasing temperature in spring the supralittoral is flushed by meltwater, followed by a period of desiccation in summer, which can be interrupted by rehydration during rain-or snow- fall (Davey 1989; Schroeter et al. 1995) or during high tides. Salinity changes strongly in the supralittoral due to the effects of tides, salt spray, desiccation, overflow with melt water and precipitation. In the eulittoral salinity rises are less strong and less frequent than in the supralittoral.

On the other hand, low salinities are quite common during low tides, precipitation and meltwater discharge. Klo¨ser (1994) determined salinities between 27 and 41 PSU in the eulittoral on King George Island. At low tide temperatures in tide pools may rise far above the coastal water temperatures up to almost 14C in summer (Klo¨ser 1994; Moore et al. 1995). Winter temperatures may be very low and depend, apart from the air

temperatures, on the thickness of the ice cover in winter.

Despite the remoteness of the polar regions pollution is an issue both in the Arctic and the Antarctic. For example, radionuclide contami- nants such as Technetium-99 (⁹⁹Tc) are present around the Arctic archipelago of Svalbard through the long-range oceanic transport of dis- charges of radioactive effluents from nuclear reprocessing plants in Europe and global fallout (Gerland et al. 2003; Gwynn et al. 2004). Another problem are oil spills. When the Argentinean ship Bahia Paraiso ran aground near Anvers Island at the Antarctic Peninsula more than 150,000 gal- lons of petroleum were released to the sur- rounding bays (Kennicutt II et al. 1990). Such oil spills can potentially cause servere harm depending on the amount and type of material released.

Biodiversity, biogeographical relationships and vertical distribution of Arctic and Antarctic seaweeds

The Arctic and the Antarctic Oceans differ considerably with respect to their genesis and their cold water history. The Southern Ocean has had no land bridge to temperate regions since the late Mesozoic and has been further separated from the neighbouring southern continents by the Antarctic Circumpolar Current since 26 Ma (Hempel 1987; Lu¨ning 1990; Kirst and Wiencke 1995). During the first major glaciation in East Antarctica 14 Ma ago water temperatures decreased and they have been low in the Southern Ocean since then (Crame 1993). In contrast, the broad shelf areas of the Arctic Ocean have had a continuous connection to the temperate coasts of America and Eurasia, and a perennial ice cover did not develop before 0.7–2.0 Ma ago (Clarke 1990). These distinctions are the major reasons for the differences in seaweed biodiversity of both polar regions.

The strong isolation of the benthic seaweed flora of the Southern Ocean has resulted in a high degree of endemism in Antarctica. 33% of all seaweed species are endemic to the Antarctic region. Within the Heterokontophyta 44% of the

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species are endemic, within the Rhodophyta 32%

and within the Chlorophyta 18% (Wiencke and Clayton 2002). There is one endemic order, the kelp-like brown algal order Ascoseirales, and there are several endemic genera: among the brown algae, Himantothallus, Cystosphaera and Phaeurus, among the red algae Gainia, Noto- phycus and Antarcticothamnion, and among the green algae Lambia and Lola (Wiencke and Clayton 2002). Well-known Antarctic endemic species include the brown algae Himantothallus grandifolius, Cystosphaera jacquinotii, the red alga Porphyra endiviifolium and the green alga Lambia antarctica. The Antarctic region is the only region in the world devoid of kelps, brown algae of the order Laminariales (Moe and Silva 1977). This order is ecologically replaced by the Desmarestiales. According to phylogenetic and morphological analyses and studies on ecophysiological traits this order is considered to have originated in the Southern Ocean and subse- quently radiated into the Northern Hemisphere (Peters et al. 1997). A conspicuous character of the Antarctic seaweed flora is the scarcity of small macroalgal epiphytes compared to temperate regions. In fact, these epiphytes are not absent, they rather occur as endophytes inside larger seaweeds, well protected against herbivory by mes- ograzers (Peters 2003). This suggests that mesoherbivory can be quite intense in Antarctica.

In contrast to the strong endemism in Antarctic macroalgae only very few endemic Arctic species have been found so far. About half a dozen species are restricted to the Arctic including the brown algae Punctaria glacialis,Platysiphon verticillatus and the red algaPetrocelis polygyna(Wilce 1990).

Most species have a distribution that extends well into the temperate region, e.g. the kelpLaminaria solidungula and the red algae Devaleraea ramentacea, Turnerella pennyi, Neodilsea integra andPantoneura baerii(Lu¨ning 1990).

Compared to rich seaweed floras like those in temperate southern Australia with about 1155 species (Womersley 1991), low species richness is characteristic for both polar seaweed floras. In the Antarctic, 119 species have been recorded so far (Wiencke and Clayton 2002) and in the Arctic there are about 150 species (Wilce 1994). These numbers are, however, likely to be underesti-

mated due to the infrequency of scientific col- lections, the extreme remoteness and logistic difficulties. In Antarctica most species occur in the Antarctic Peninsula region and only very few species are recorded at the southernmost distribution limit in the Ross Sea. A similar decrease in species richness has been detected in East Greenland between Scoresby Sound, Franz Josephs Fjord and Jo¨rgen Bro¨nlunds Fjord (70, 74 and 82N, respectively; Lund 1951, 1959a, b). On the panarctic level, macroalgal species richness seems to dramatically decrease from the western (Atlantic) sector to the eastern (Pacific) sector.

While about 70 species have been recorded from the Svalbard region (Weslawski et al. 1993, 1997;

Vinogradova 1995), only about 10 species are known from the rocky littoral regions in the Alaskan Beaufort Sea (Dunton and Schonberg 2000).

As a result of the strong effect of the Antarctic Circumpolar Current on the dispersal of seaweed propagules (Lu¨ning 1990) many non-endemic species of the Antarctic seaweed flora have a circumpolar distribution. Among the species also occurring on sub-Antarctic islands and Tierra del Fuego are the red algaIridaea cordata, the brown algaGeminocarpus geminatusand the green alga Monostroma hariotii. Some species, e.g. the red alga Ballia callitricha and the brown alga Adenocystis utricularis, even occur in New Zea- land and Australia. A similar connection between the Antarctic and the cold temperate region of South America has also been recorded for marine invertebrates (Clarke et al. 2005). At least 20 algal species from the Antarctic are cosmopolitan, e.g. the red alga Plocamium cartilagineum, the brown alga Petalonia fascia and the green alga Ulothrix flacca (Papenfuss 1964; Wiencke and Clayton 2002). It is possible that some such species may be recent invaders from temperate regions (Clayton et al. 1997).

A few seaweed species have a disjunct amphiequatorial distribution and occur both in the Antarctic and the Arctic, e. g.Acrosiphonia arcta and Desmarestia viridis/confervoides. Molecu- lar studies indicate that the biogeographic disjunctions of these species are recent and probably date back to the maximum of the Wu¨rm/Wisconsin glaciation 18,00 years ago (van

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Oppen et al. 1993). The units of dispersal were certainly the microscopic stages in the life cycle because they are more resistant to high temperatures allowing the possibility of a passage through the tropics during times of lowered water temperatures (Peters and Breeman 1992;

Wiencke et al. 1994; Bischoff and Wiencke 1995a).

Apart from the few species endemic to the Arctic and various cosmopolitan species such as the red alga Audouinella purpurea, the brown alga Scytosiphon lomentaria and the green alga Blidingia minima, the Arctic seaweed flora has affinities to the Atlantic, the Pacific and the Indo-Pacific region (Wilce 1990). An example of an invader from the Pacific may beAcrosiphonia arcta. Populations of this species from the Arctic and the North Atlantic seem to originate from the Pacific according to molecular studies (van Oppen et al. 1994). But over 90% of the species in the Arctic originate from Atlantic populations (Dunton 1992). This is particularly obvious in regions with strong influx of Atlantic waters, e.g.

in Svalbard (Svendsen et al. 2002, Hop et al.

2002). However, even in the coastal areas of the Beaufort Sea there is a strong Atlantic influence, marked by the kelps Laminaria solidungula and Alaria esculenta (Dunton 1992) while the Cana- dian Arctic also has a high proportion of macroalgae of Pacific origin (Cross et al. 1987).

In both polar regions seaweeds are almost entirely subtidal. However, there are some spe- cialized species with a bipolar distribution that occur exclusively in the supralittoral, i.e. in the spray zone. These are the green alga Prasiola crispa, which also grows more inland close to seabird rockeries under conditions of low pH and high nutrient concentrations (Knebel 1936) and the red alga Bangia atropurpurea (Bird and Mc Lachlan 1992; Clayton et al. 1997). The green alga Urospora penicilliformis and species of the genus Ulothrix grow just around the high tide level both in the Antarctic and the Arctic.

Acrosiphonia arcta is a species typical for the lower eulittoral in both polar regions.

A conspicuous species in the upper eulittoral in the Antarctic is the red alga Porphyra endiviifolium and in the lower eulittoral/upper sublittoral the green alga Enteromorpha bulbosa and the brown alga Adenocystis utricularis are

common (Westermeier et al. 1992; Wiencke and Clayton 2002). Tide pools and crevices in the lower sublittoral are often colonized by upper sublittoral species such as the red algaePalmaria decipiensandIridaea cordata. The upper 5–15 m of the sublittoral are exposed to ice floes and are often devoid of large, perennial algae. Only crustose species or developmental stages can persist here. Below this zone, large brown algae dominate the sublittoral in West Antarctica:As- coseira mirabilisandDesmarestia menziesiioccur in the upper sublittoral, D. anceps in the mid sublittoral andHimantothallus grandifoliusgrows in the lower sublittoral (DeLaca and Lipps 1976;

Lamb and Zimmermann 1977; Amsler et al. 1995;

Klo¨ser et al. 1996; Quartino et al. 2001, 2005). At higher latitudes in East Antarctica only few species occur, in particular Palmaria decipiens, Phyllophora antarctica and I. cordata (Zaneveld 1968; Miller and Pearse 1991; Cormaci et al.

1992).

In the Arctic the barren zone heavily exposed to floating ice extends down to about 2 m water depth. The upper sublittoral on Spitsbergen is characterized by the brown algaeFucus distichus, Pylaiella littoralis, Chordaria flagelliformis, the kelp Saccorhiza dermatodea, the red alga Devaleraea ramentacea and green algae of the genusAcrosiphonia. The zone below is dominated by the kelpsAlaria esculenta,Laminaria digitata and L. saccharina. Characteristic for the lower sublittoral are the red algaePhycodrys rubensand Ptilota gunneri. The Arctic kelp, L. solidungula, occurs in this zone as well but only in the inner part of the fjords (Svendsen 1959; Hop et al. 2002;

Wiencke et al. 2004). The seaweed vegetation in the Canadian Arctic (Baffin Island) is similar to that in Spitsbergen with a shallow F. distichus zone, the upper sublittoral characterized byStic- tyosiphon tortilis, P. littoralis and Dictyosiphon foeniculaceus (Cross et al. 1987). Deeper communities are dominated by the kelps L. saccharina, L. solidungula, A. esculenta and Agarum cribrosum, interspersed with the red algaeDilsea integra,D. ramentaceaandRhodomela confervoides. In contrast, no supralittoral or intertidal algae have been recorded from the Alaskan Beaufort Sea. Here, algae are restricted to scattered rocky habitats in shallow waters (about

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5–10 m), which are protected by barrier islands from iceberg scouring. Laminaria solidungula is the dominant kelp species, althoughAlaria escul- entaandL. saccharinacan also be found regularly (Dunton and Schonberg 2000). Characteristic red algal species are Phycodrys rubens, Odonthalia dentata,Dilsea integra,Phyllophora truncata and Rhodomela subfusca. Exposed rock is usually covered by encrusting coralline red algae, Litho- thamnionspp. (Konar and Iken 2005).

Reproductive and physiological thallus anatomy

The enigma of reproduction and life histories of endemic Antarctic Desmarestiales and of Ascoseira mirabilis has been clarified. The sorus structure ofH. grandifolius(Moe and Silva 1981;

Wiencke and Clayton 1990),D. anceps(Moe and Silva 1981; Wiencke et al. 1996) andD. antarctica (Moe and Silva 1989; Wiencke et al. 1991) is similar, indicating an evolutionary relationship.

Unilocular sporangia are cylindrical, borne ter- minally on 2–4 celled stalks and are interspersed with paraphyses composed of 2–4 cells with many physodes. With respect to sorus morphology, D.

menziesiiexhibits a closer similarity to the Arctic cold-temperate species D. aculeata (Wiencke et al. 1995), whereas Phaeurus antarcticus resembles the North Atlantic-Mediterranean species Arthrocladia villosa (Clayton and Wie- ncke 1990). InP. antarcticus, sporangia are cate- nate and develop in rows in adjacent cells as filamentous outgrowths of the cortex, interspersed with club-shaped sterile hairs. These phylogenetic relationships have been confirmed meanwhile by molecular data (Peters et al. 1997).

Ascoseira mirabilis, whose exact phylogenetic relationships are still unresolved, has a fucalean type of life history (Clayton 1987). There is one free-living diploid generation with conceptacles scattered over both surfaces. These contain den- sely packed chains of gametangia that release biflagellate isomorphic gametes. Zygotes develop into new individuals.

A striking feature of several Antarctic Des- marestiales and A. mirabilis is their anatomical complexity resembling that of Laminaria species from the northern Hemisphere. As far as we

know today these taxa are characterized by a highly diversified structure and complex morpho- functional processes including a temporal syn- chronization between photosynthesis and growth as well as the long-distance transport of organic substances (Lu¨ning et al. 1973; Schmitz 1981;

Clayton and Ashburner 1990; Drew and Hastings 1992; Go´mez et al. 1996). Such characteristics represent strategies to cope with the marked seasonality in polar and cold-temperate regions (Chapman and Lindley 1980; Go´mez and Wiencke 1998; Go´mez and Lu¨ning 2001).

As in other species ofLaminaria the blade of L. solidungula has a basally located meristem, which is active only in winter and forms—comparable withL. hyperborea—a new blade at the distal end (Taylor 1966; Dunton and Jodwalis 1988). Up to three generations of blades may be found in one individual. As in species of Lami- naria, blades ofHimantothallus grandifoliusgrow in their lower part (Dieckmann et al. 1985; Drew and Hastings 1992). Punch-hole experiments with A. mirabilis indicate that the blade elongates longitudinally as in Laminaria solidungula through a seasonally active intercalary meristem (Go´mez et al. 1995a).

Carbon fixation rates in kelps and kelp-like brown algae differ between blade parts (Arnold and Manley 1985; Go´mez et al. 1995a, b; Cabello- Pasini and Alberte 2001). During the growth phase in late winter-spring, net photosynthetic rates (net Pmax) inA. mirabilisare slightly higher in the middle region compared to the basal and distal regions (Go´mez et al. 1995a). In comparison, inL. solidungula, C-fixation rates are lowest in meristematic tissue, highest in first year tissue and intermediate in second-blade tissue (Dunton and Jodwalis 1988). This pattern is related to the ontogeny within the blade, i.e. photosynthetic activity increases with age of the tissues reaching a maximum but then decreases with further aging.

In apical regions, erosion and senescence take place.

Over the years, the blade inAscoseirabecomes thicker and more complex as new tissue is formed each growth season, resulting in modifications not only of the photosynthetic gradients but also of the photosynthetic capacity and efficiency along the thallus. Two age-components must be

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considered here: The age of the different blade tissues and the age of the whole plant. In this context, 2-year old plants of Ascoseira are characterized by net Pmax and a-values almost twice that of 3-year old individuals. However, other parameters such as dark respiration, saturation (Ek) and compensation (Ec) points do not show obvious differences (Go´mez et al. 1996).

The photosynthetic variability correlated with tissue age may also be seen in terms of the development of the photosynthetic apparatus with ontogeny. In both age classes, middle regions have a higher net Pmaxthan basal and distal regions, suggesting that photosynthesis is low due to the presence of a non-developed photosynthetic apparatus in the basal region, and decreases in the oldest distal tissues due to senescence processes.

Similar results were obtained in young and adult plants of L. solidungula (Dunton and Jodwalis 1988).

Ku¨ppers and Kremer (1978) associated the increased¹⁴C-assmilation in the middle and distal regions ofLaminariaspecies with a higher activity of the Calvin cycle enzyme ribulose 1,5-bis- phosphate carboxylase-oxygenase (RUBISCO).

Moreover, these authors demonstrated longitu- dinal profiles in light independent C-fixation in these species coupled to a high activity of the enzyme phosphoenolpyruvate carboxykinase (PEP-CK) in the meristematic region (b-carboxylation). The activities of these carboxylating enzymes apparently respond to the growth characteristics of Laminaria. In fact, Laminaria species from cold-temperate and Arctic regions grow in winter or in dim light and it is likely that such an alternative carboxylating mechanism is advantageous for these species (Ku¨ppers and Kremer 1978). b-carboxylation is also linked to the growth requirements of these algae. For example, light-independent carbon fixation pro- vides C-skeletons (preferentially amino-acids) for both biosynthesis and anabolic processes, thus replenishing some carbon intermediates in e.g.

the Krebs cycle (Kremer 1981b; Falkowski and Raven 1997). Particularly, in the meristematic region of Laminaria, PEP-CK uses CO2 lost in glycolysis of mannitol translocated from the distal region to the meristem (Kremer 1981a; Kerby and Evans 1983).

The patterns of C-fixation inAscoseira exhibit also intra-blade variations (Go´mez et al. 1995a) although some differences with respect to patterns reported in Laminaria are observed. Both light dependent and light independent C-fixation increase with tissue age reaching a maximum in the middle/distal parts of the blade. In contrast, members of the Laminariales studied to date show highest rates of light dependent carbon fixation in distal and highest light independent C fixation in the basal parts (Ku¨ppers and Kremer 1978). The different thallus allocation of light independent C fixation in A. mirabilis may be related to the high dark respiration rates observed in distal blade regions (Go´mez et al. 1995a, 1996).

It is not clear, however, whether light independent C-fixation may compensate for C losses due to respiration as reported by Kremer (1981b).

Thomas and Wiencke (1991) could not conclu- sively demonstrate a relationship between light independent C-fixation and dark respiration in Antarctic marine algae. In general, dark C-fixation varied between 4.9% and 31% of dark respiration in five brown algae and one red alga.

In species such asH. grandifoliusand D. anceps, low dark C-assimilation rates were coupled to high respiration rates as inAscophyllum nodosum indicating a net C loss due to respiration in the dark (Johnston and Raven 1986).

In kelps sugars are synthesized and stored as polysaccharides (e.g. laminaran) in the middle and distal assimilatory tissues of the algae, from which they are then translocated as low-molecular-weight compounds (e.g. mannitol) in trumpet hyphae to the growth region (Kremer 1981a, b).

The trumpet hyphae of Laminariales are elon- gated, longitudinally oriented cells in the medulla with trumpet like ends. The cross walls are per- forated by numerous pits resembling the sieve plates of sieve tubes in higher plants (Schmitz 1981, 1990; Buggeln 1983). Similar trumpet hyphae are present in the medulla ofH. grandifolius (Moe and Silva 1981) and in the other Desma- restialesPhaeurus antarcticus (Clayton and Wie- ncke 1990), Desmarestia antarctica (Moe and Silva 1989; Wiencke et al. 1991) andD. menziesii (Scrosati 1992; Wiencke et al. 1995). The trumpet hyphae can be interconnected by sieve plates and are always surrounded by numerous small cells

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that probably function as transfer cells. In A. mirabilis longitudinally arranged ‘‘conducting channels’’ comparable to the trumpet cells found in Laminariales are present in the medulla (Clayton and Ashburner 1990). The channels are aseptate, multinucleate structures with ensheath- ing filaments often interconnected through sieve- like wall perforations. Although no conclusive evidence for a possible transport function of the conducting channels in A. mirabilis is available, differential allocation of reserve carbohydrates associated to meristem activity strongly suggest the involvement of these structures in long distance transport (Go´mez and Wiencke 1998).

Overall, the findings that photosynthesis and carbon allocation vary as a function of blade development add new evidence to a convergent morpho-functional evolution between large Antarctic brown algae and Laminariales of the northern Hemisphere. In this case not only morphological organization, but also the metabolic differentiation along the blade, are common characteristics of the taxa. Such characteristics certainly reflect adaptive mechanisms to with- stand resource limitation in seasonally changing environments, which have ultimately led to the ecological success of these algae in polar regions.

Temperature demands and geographical distribution

Photosynthesis of polar seaweeds shows a considerable adaptation to the low temperatures of the environment. Maximum photosynthetic rates of endemic Antarctic species are at a temperature of 0C similar to values from temperate species measured at higher temperatures (Drew 1977;

Thomas and Wiencke 1991; Wiencke et al. 1993;

Weykam et al. 1996; Eggert and Wiencke 2000).

Moreover, the temperature optima for photosynthesis at least in some species from the Antarctic are well below values determined in temperate species. The lowest temperature optima have been determined in the brown algae Ascoseira mirabilis (1–10C) and Himantothallus grandifolius (10–15C; Drew 1977; Wiencke et al. 1993).

The red algae Ballia callitricha and Gigartina skottsbergii also exhibit values between 10 and

15C, whereas Kallymenia antarctica, Gymno- gongrus antarcticusandPhyllophora ahnfeltioides exhibit broad optima between 10 and 20 (to 25)C (Eggert and Wiencke 2000). Studies on the few Arctic seaweeds show a temperature optimum at 20C (Healey 1972). For comparison, in cold-and warm-temperate species optimum values of 20–25C and 25–35C were determined, respectively (Lu¨ning 1990). The temperature optima for respiration are clearly above the optima for photosynthesis but temperatures higher than 30C have never been tested in Antarctic seaweeds (Drew 1977; Wiencke et al. 1993; Eggert and Wiencke 2000). Photosynthesis:respiration ratios are highest at the lowest tested temperature, 0C, and decrease with increasing temperatures due to different Q10 values for photosynthesis (1.4–3.5) and respiration (2.5–5.1).

The high P:R ratios at low temperatures are the major reason for the high growth rates of Antarctic species at low temperatures. In particular red and brown algal species from both polar regions exhibit temperature growth optima at 0–5C or even at –2C (Wiencke and tom Dieck 1989, 1990; Novaczek et al. 1990; Bischoff and Wiencke 1993; Bischoff-Ba¨smann and Wiencke 1996; Eggert and Wiencke 2000; McKamey and Amsler 2006). Some species likeGeorgiella con- fluens, Gigartina skottsbergii and Plocamium cartilagineum from the Antarctic grow only at 0C, the lowest temperature tested, but not at 5C (Bischoff-Ba¨smann and Wiencke 1996). The upper survival temperatures (USTs), determined after 2-week-exposures to different temperatures, are as low as 7–11C. Other Antarctic red algae grow up to 5C or 10C and have USTs of£19C (Bischoff-Ba¨smann and Wiencke 1996). The sporophytes of endemic Antarctic Desmarestiales grow up to 5C and exhibit USTs of 11–13C. In contrast, their gametophytes grow up to 10C or 15C and have USTs between 15C and 18C (Wiencke and tom Dieck 1989, 1990). The upper limit for gametogenesis (ULG) inD. antarcticais 5C (Wiencke et al. 1991). Antarctic cold-temperate species (especially from the eulittoral) have higher temperature requirements. They grow up to 10–15 (or 20)C and show USTs between 13.5C and 19C. Microthalli of Antarctic cold-temperate brown algae exhibit

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USTs between 21C and 25C and ULGs between 13C and 15C (Wiencke and tom Dieck 1990;

Peters and Breeman 1993).

As far as we know today the temperature demands for growth of Arctic seaweeds are some- what higher than endemic Antarctic species. It must, however, be pointed out that the temperature demands of truly endemic Arctic species (see chapter 3) have not been investigated so far. The sporophyte of the kelp Laminaria solidungula, whose distribution extends into the cold-temperate region as far as Newfoundland, grows at temperatures up to 15C with an optimum at 5–10C and USTs of 16C (tom Dieck 1992). The male and female gametophytes of this species exhibit an UST of 18C and lower survival temperatures (LSTs) of £–1.5C (Bolton and Lu¨ning 1982; tom Dieck 1993). The red alga Devaleraea ramentacea, which is distributed from the Arctic to the cold temperate North Atlantic region, grows at up to 10C with an optimum at 0C and exhibits an UST of 18–20C and an LST of£–5C.

The ULG of this species is 8C (Novaczek et al.

1990; Bischoff and Wiencke 1993). Macrothalli of species with a prominent distribution in both, the Arctic and the cold-temperate region, grow at up to 15 or 20 (to 25)C with optima between 5 and 15 (to 20)C and exhibit USTs between 17 and 25 (to 26)C. The LSTs are £–1.5 or 2C (Wiencke et al. 1994). The microscopic gametophytes of Arctic cold-temperate Laminariales grow at up to 20C and have USTs between 22 and 25 (to 28)C. Gametophytes of Alaria esculenta and Agarum cribrosum, however, exhibit USTs of 19–

21C, as low as those of the more Arctic species Laminaria solidungula. The LSTs are either 0, –1.5 or –2C, the few data on ULGs vary between 10C and 17C (Wiencke et al. 1994).

The northern distribution of endemic Antarctic species is often limited by the temperature demands for growth. This applies especially to members of the endemic Antarctic species of the order Desmarestiales. In these taxa the northern distribution limit is determined by the temperature requirements for growth of the sporophytes (Wiencke and tom Dieck 1989), which occur only south of the Antarctic convergence in areas with maximum temperatures £5C allowing growth of their sporophytes. The USTs of their sporophytes

and gametophytes as well as the temperature demands for growth of the gametophytes are irrelevant for the explanation of the geographic distribution of these species.

The distribution of Arctic North Atlantic species is often limited both by the USTs and the ULGs (van den Hoek 1982a, b; Breeman 1988;

Lu¨ning 1990). In such taxa, distribution limits in the West Atlantic are determined by lethal, high summer temperatures, whereas they are determined in the East Atlantic by high winter temperatures inhibiting reproduction. Examples for species from this group are Laminaria digitata, Chorda filumandHalosiphon tomentosus.

During the ice ages both polar regions were inhospitable for seaweeds. In the Southern Hemisphere the sub-Antarctic islands probably served as refugia. The South American Archipel- ago may also have hosted species escaping from the coasts of the Antarctic continent (Skottsberg 1964). At the maximum of the last ice age the 5C summer isotherm, the boundary of the Antarctic region just touched the southern tip of South America (CLIMAP project members 1981).

Migration of species from the Antarctic continent to South America and vice versa probably occurred along the Scotia Arc, a well-recognized route for animals (Knox and Lowry 1978). In the Northern Hemisphere cold water seaweeds of the Atlantic with ULGs and upper temperature limits for growth at 10 or 15C experienced an extreme reduction in the distribution area during the ice ages (van den Hoek and Breeman 1989). The distribution of these species was compressed by the glaciers in the North and the 10–15C winter isotherm, their southern reproduction boundary.

This is the likely explanation for the present depauperate flora in the North West Atlantic.

Comparable conditions did not exist in the North Pacific, probably a major reason for the richness of the cold North Pacific.

During periods of lowered temperatures taxa with relatively high temperature demands were able to extend their distribution limits towards the equator. Species with an amphiequatorial distribution e.g.Acrosiphonia arcta(Bischoff and Wiencke 1995a),Urospora penicilliformis(Bischoff and Wiencke 1995b) and Desmarestia viridis/

confervoides (Peters and Breeman 1992) have

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probably crossed the equator during the Pleisto- cene lowering of the water temperatures in the tropics (Wiencke et al. 1994). The USTs of these taxa are with 25–27C slightly above the mini- mum tropical sea surface temperatures of 23–25C during the last glaciation (CLIMAP Pro- ject members 1981). These results are supported by molecular studies indicating an almost complete sequence identity in amphiequatorial populations ofA. arctaandD. viridis/confervoidesin the fast- evolving internal transcribed spacer regions of the ribosomal DNA (van Oppen et al. 1993).

Light demands and depth zonation

At high latitudes, the radiation regime imposes severe constraints not only in terms of seasonal light availability but also in regard to the vertical distribution of benthic algae (Go´mez et al. 1997).

Because of the extreme environmental conditions in the eulittoral, polar algae are mainly sublittoral and thus low light demands and tolerance to darkness are a pre-requisite for occurrence down to great depths (Arnoud 1974; Zielinski 1981;

Richardson 1979; Klo¨ser et al. 1993; Amsler et al.

1995). An important feature is the dark tolerance of the microscopic developmental stages. Various Antarctic and Arctic seaweeds tolerate a dark period of up to 18 months (tom Dieck 1993;

Wiencke 1988, 1990a). Further evaluation of the relation between photosynthetic characteristics and algal zonation in 36 macroalgal species from King George Island (Weykam et al. 1996, Go´mez et al. 1997) indicates a high degree of shade adaptation: (a) photosynthetic efficiency (a) is high in all the studied species, reflecting a clear shade adaptation over a broad range of depth;

(b) seaweeds growing at depths >10 m exhibit low saturation points for photosynthesis (Ek; < 40 lmol m^–2s^–1) irrespective of their taxonomic position; (c) the highest Ek values (>50lmol m^–2s^–1) are found in species common in upper sublittoral or eulittoral; (d) shallow water species have higher photosynthetic capacity (Pmax) than species from deeper waters. These data obtained using field material are supported also by results obtained in studies using specimens grown from unialgal cultures from the same study area

(Wiencke et al. 1993; Eggert and Wiencke 2000).

The highest degree of shade adaptation with average Ek values around 3lmol m^–2s^–1 has been demonstrated in coralline algae from the Ross Sea (Schwarz et al. 2005).

The vertical distribution of dominant Antarctic seaweeds such asDesmarestiaor Himantothallus can be extremely wide in contrast to the algal zonation patterns from cold-temperate and temperate regions, where zonation patterns are characterized by narrow belts of species (Lu¨ning 1990). However, no evidence of an acclimation to the prevailing light conditions at different depths could be demonstrated in five species of seaweeds along a depth gradient between 10 m and 30 m (Go´mez et al. 1997). Apparently, the intrinsic low light requirements for photosynthesis account for these patterns. In the Antarctic spring-summer, due to high water transparency irradiances of PAR around 20lmol m^–2s^–1reach the depth of 30 m, with 1% of the surface irradiance present at depths >40 m (Go´mez et al. 1997). Although these levels are clearly lower than average midday irradiances (30–325lmol photon m^–2s^–1) at 30 m in some clear temperate and tropical waters (Peckol and Ramus 1988), they exceed reported saturation and compensation points of photosynthesis in many Antarctic seaweeds (Weykam et al. 1996).

As for photosynthesis, the light demands for growth are similarly very low. In microscopic developmental stages of Antarctic seaweeds growth is light saturated already at 4–12lmol m^–2s^–1(Wiencke 1990a). In young sporophytes of Antarctic Desmarestiales growth is saturated at 15–20lmol m^–2s^–1(Wiencke and Fischer 1990).

In the case of Arctic species, low light requirements for photosynthesis have also been found in nine species from Spitsbergen (Latala 1990) and in crustose coralline red algae from the high Arctic (Roberts et al. 2002). Meristematic tissue of both juvenile and adult individuals of Laminaria solidungula from the Alaskan high Arctic exhibits Ek values between 20 and 30lmol m^–2s^–1, while the average Ek value of vegetative blade tissue in adult plants is 38lmol m^–2s^–1 (Dunton and Jodwalis 1988).

Photosynthetic efficiency (a) is higher than in Laminariales from the temperate region. Both the

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low Ekandavalues indicate strong adaptation to the long period of exposure to darkness in winter under ice cover and in summer during times of high water turbidity. Another feature characte- rising the dark adaptation ofL. solidungulais the low compensation point (Ec) for growth close to 0.6lmol m^–2s^–1(Chapman and Lindley 1980).

Seaweeds able to grow in deep waters have developed metabolic strategies to maximize carbon fixation by avoiding excessive carbon losses due to respiration. Because at great depths, Ecfor photosynthesis exceed Ec values for growth and available irradiances are normally below the levels required for saturation of photosynthesis, carbon assimilation may be just compensating dark respiration. In Antarctic brown algae, dark respiration has a strong seasonal component and during the growth period, respiratory activity may account for a considerable proportion of the gross photosynthesis (Go´mez et al. 1995a, b). If one relates the daily light course of the irradiance to the Ek value, then the daily period for which plants are exposed to irradiances >Ek (denomi- nated Hsat) can be estimated. The obtained metabolic daily carbon balance can be regarded as a physiological indicator for the ability to grow in deep waters (Go´mez et al. 1997).

Polar seaweeds exposed to marked seasonal changes in daylength exhibit generally Hsat

values >0 h only during the short open water season. Laminaria solidungula in a kelp bed in the Alaskan Beaufort Sea at 70 N was exposed during August to September 1986 to total Hsatperiods of up to 148 h (Dunton 1990). This value corresponds to an average daily Hsat of 3 h. However, depending on the year, the average daily Hsatmay decrease down to < 0.5 h. Year-round underwater light measurements have yielded annual quantum budgets of 45 mol m^–2yr^–1, the lowest ever docu- mented for kelp populations globally (Dunton 1990). A similar low value, 49 mol m^–2 yr^–1, was already obtained earlier by Chapman and Lindley (1980), values considerably lower than in the temperate L. hyperborea, which receives 71 mol m^–2yr^–1(Lu¨ning and Dring 1979).

For Antarctic seaweeds, Hsatmeasured during optimum light conditions in spring in five brown and red algae decreases with depth from values close to 14 h at 10 m to values between 7 h and

12 h at 30 m depth (Go´mez et al. 1997). For the red algaePalmaria decipiens,Kallymenia antarc- ticaandGigartina skottsbergiia metabolic carbon balance between 0.6 and 0.8 mg C g^–1FW d^–1sets the limits for growth at >30 m. For Himanto- thallus grandifolius, which dominates depths below 15 m, the daily carbon balance was low but relatively similar over a range between 10 m and 30 m, indicating that this species can potentially grow even considerably deeper. Only in Des- marestia ancepsis growth clearly limited at 30 m due to its negative carbon balance at this depth (–1.9 mg C g^–1FW d^–1; Go´mez et al. 1997). The lower depth distribution limit of the red alga Myriogramme mangini from the South Orkney Islands has been predicted by photosynthetic measurements to be at 23 m water depth (Brouwer 1996).

Overall, polar seaweeds by virtue of their low light demands are potentially able to grow over large ranges of depths. Depending on the water characteristics the lower depth distribution limit of seaweeds both in the Antarctic and the Arctic is located between 30 m and 90 m (Wilce 1994;

Wiencke and Clayton 2002). However, other constraints such as competition also control algal zonation. For example, red algae are metabolically able to live at great depths, however, they can be outcompeted by the large canopy brown alga Himantothallus(Klo¨ser et al. 1996). Furthermore, ice abrasion and grazers, e.g. some invertebrate and demersal fishes, have a strong influence on zonation patterns (Iken 1996; Iken et al. 1997).

Antarctic seaweeds are not only strongly shade- adapted but can also cope with high light conditions in summer due to their ability for dynamic photoinhibition, a photoprotective mechanism by which excessive energy absorbed is rendered harmless by thermal dissipation (Krause and Weis 1991; Demmig-Adams and Adams III 1992). This capability is best expressed in species from the eulittoral. Upper and mid sublittoral species show a more or less pronounced decrease in photosynthetic activity during high light stress and full recovery during subsequent exposure to dim light (Hanelt et al. 1997). In contrast, deep water and understory species recover only slightly and slowly, indicating photodamage. Similar findings as these on Antarctic seaweeds have been demonstrated

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also in a detailed analysis of seaweeds from Spits- bergen (Hanelt 1998). Similarly, UV radiation is now also regarded as a key factor affecting the depth zonation of seaweed assemblages. This topic will be treated in detail in a separate paper in this issue (Bischof et al. in press).

Effect of salinity, temperature and desiccation on supra-and eulittoral seaweeds

Until now few ecophysiological studies have been undertaken on the salinity acclimation in polar seaweeds (Karsten et al. 1991a, b; Jacob et al. 1991, 1992a). These papers indicate that cells of eulittoral Chlorophyta from the Antarc- tic survive salinities between 7 psu and 102 psu with a low rate of mortality, and that most taxa grow, photosynthesize and respire optimally under normal seawater conditions with rather broad tolerances between 7 psu and 68 psu. The supralittoral Prasiola crispassp. antarctica even grows between 0.3 psu and 105 psu. Consequently, eulittoral and supralittoral macroalgae from Antarctica can be characterized as euryhaline organisms.

Osmotic acclimation in response to salinity changes is a fundamental mechanism of salinity tolerance that conserves intracellular homeostasis (Kirst 1990). The acclimation process in Antarctic Chlorophyta involves the metabolic control of the cellular concentrations of osmolytes. The major inorganic osmolytes are potassium, sodium and chloride (Karsten et al. 1991b; Jacob et al. 1991), the cellular concentrations of which can be rapidly adjusted with low metabolic energy costs, especially compared to the cost of organic osmolyte biosynthesis or degradation (Kirst 1990).

However, protein and organelle function, enzyme activity and membrane integrity in seaweeds are adversely affected by increased electrolyte con- centration. Hence, the biosynthesis and accumulation of organic osmolytes in the cytoplasm permits the generation of low water potentials without incurring metabolic damage. For these organic compounds that are tolerated by the metabolism even at high intracellular concentrations, the term ‘compatible solute’ was introduced by Brown and Simpson (1972).

All Antarctic Chlorophyta studied possess as main organic osmolytes the carbohydrate sucrose and the imino acid proline, and—with the exception of Prasiola—a third compound, b-dimethylsulphoniumpropionate (DMSP).

Prasiola is able to synthesize polyols such as sorbitol and ribitol instead of DMSP. The concentrations of all osmolytes are actively regulated as a function of the external salinity. Because of its physicochemical properties proline is one of the most potent organic osmolytes, which not only balances salinity stress, but also may stimulate enzymatic activity. This imino acid is the most important osmolyte in ice-algae too (Tho- mas and Dieckmann 2002). Sucrose is also a well- known osmotically active compound in many higher and lower plants, and also exhibits a cryoprotective function. The osmotic function of DMSP seems to be unique to Antarctic Chloro- phyta in comparison with temperate ones, because of very high intracellular concentrations and the strong biosynthesis and accumulation with increasing salinities. In addition, DMSP acts as compatible solute and cryoprotectant (Karsten et al. 1996a). Polyols such as sorbitol are the most water-like molecules, and therefore represent not only ideal osmolytes and compatible solutes, but exert a function as rapidly available respiratory substrate (e.g. under desiccation) and as antioxi- dant (Karsten et al. 1996b). The presence of high concentrations of three organic osmolytes in Antarctic Chlorophyta may be related to the extremely cold habitat suggesting that, besides their osmotic role, these solutes are playing mul- tiple functions in metabolism such as cryoprotectants. In the case ofP. crispassp.antarcticathe broad salinity tolerance is also assisted by the thickness and mechanical properties of the cell walls (Jacob et al. 1992a). Another ultrastructual feature ofPrasiolacells is the absence of vacuoles under hypososmotic conditions up to full seawater and the formation of vacuoles at high salinities. Under the latter conditions, they may serve as compartments accumulating inorganic ions.

Compared to the eulittoral Chlorophyta, much less is known of the ecophysiology of the red algae Bangia atropurpurea and Porphyra endiviifolium from Antarctica. The few data on temperature requirements for growth and

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survival indicate eurythermal characteristics for both Rhodophyta, i.e. they survive temperatures up to 21–22C (Bischoff-Ba¨smann and Wiencke 1996). Studies on closely related species of both genera from other biogeographic regions clearly indicate an extremely broad tolerance of all environmental factors, which is based on a high metabolic flexibility (Karsten et al. 1993; Karsten and West 2000). BangiaandPorphyrasynthesize and accumulate three isomeric heterosides with different physiological functions as osmolytes, compatible solutes and soluble carbon reserve.

Besides hypersaline conditions decreasing temperatures also strongly stimulate the biosynthesis and accumulation of DMSP in Antarctic Chlorophyta (Karsten et al. 1996a). In addition, DMSP not only stabilises the cold-labile model enzyme lactate dehydrogenase and malate dehydrogenase extracted from Acrosiphonia arcta during several freezing and thawing cycles, but also stimulates both enzyme activities at in situ concentrations. Consequently, DMSP acts as an effective cryoprotectant (Nishiguchi and Somero 1992). Recent studies on Antarctic Prasiola and sea ice diatoms indicate the presence of ice-bind- ing proteins (IBP) that modify the shape of growing intracellular ice crystals during freezing (Raymond and Fritsen 2001). IBPs do not lower the freezing point, they rather seem to prevent damage to membranes by the inhibition of the recrystallization of ice (Raymond and Knight 2003). During recrystallization small ice particles typically grow to large grains of ice, which may physically injure cell membranes. Consequently, IBPs act as effective structural cryoprotectants.

In the eulittoral and supralittoral zone, low temperatures combined with high irradiance represent a particular challenge to algal physiol- ogy. At low temperature, and, thus, reduced enzyme activities and decreased turn-over velocity of D1 reaction centre protein in photosystem II (Davison 1991; Andersson et al. 1992; Aro et al.

1993), a persisting high irradiance of PAR may result in increased electron pressure in photosynthesis. This may ultimately result in the generation of reactive oxygen species within the Mehler reaction (Polle 1996) and increase oxidative stress (Asada and Takahashi 1987).

The consequences of increased oxidative stress

are chronic photoinhibition/photoinactivation, bleaching of photosynthetic pigments, peroxida- tion of membrane lipids and enhanced degradation of D1 protein (Aro et al. 1993; Osmond 1994). Hitherto this phenomenon is hardly studied in Antarctic macroalgae (Hanelt et al. 1994, 1997). However, the limited information available suggests that polar algae from the eulittoral, such as the brown alga Adenocystis utricularis, may overcome radiation stress at low temperatures by their ability for dynamic photoinhibition/photoprotection (Osmond 1994), which proceeds much faster than in sublittoral algae (Hanelt et al. 1994, 1997). The rate of inhibition seems to be independent of temperature. The underlying mechanism is still unexplored, but possible explanations include the adaptation of enzymes involved in the D1 repair cycle at low temperatures, and the insignificant role of D1 in photoinhibition and recovery of photosynthesis in Antarctic macroalgae (Hanelt et al. 1994). The ability for fast photoinhibition and to completely halt photosynthesis under steadily decreasing temperatures at constant irradiance levels was also found in eulittoralFucus distichusfrom Arctic Spitsbergen (Bischof and Walter, unpublished data). Here, a critical temperature level to initiate pronounced photoinhibition was found to be –3C. As soon as temperatures fall below this threshold, photosynthesis becomes rapidly inhibited, and photosynthetic quantum yield completely ceases at –15C. Recovery from freezing temperature proceeds almost in reverse, with a rapid increase in quantum yield as soon as temperatures climb above –3C. By their ability to reduce photosynthetic quantum yield, polar eulittoral algae seem to be able to avoid increasing oxidative stress under low temperature conditions. However, some species seem to apply other strategies of photoprotection under low temperature, since Becker (1982) reported for Antarctic Prasiola photosynthetic activity down to –15C. The capacity to photosynthesize as efficiently in air (when hydrated) as in water, in combination with a high affinity for inorganic carbon, has been described for a temperate species of this genus (Raven and Johnston 1991).

Desiccation is a strong stress parameter in supralittoral species. Air exposed thalli of

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Prasiola crispa loose 75% of the cellular water during the first 6 h of desiccation (Jacob et al.

1992b). A water loss of more than 90% leads to irreversible damage. Growth rates after reim- mersion in seawater depend on the thallus water content and the length of the desiccation period.

Few ultrastructural changes were found after desiccation. As after salinity stress, the very thick cell walls of the species and the absence of vacuoles are regarded as prerequisites to survive periods of desiccation (Jacob et al. 1992b).

Although there is a lack of knowledge of the ecophysiological performance of many eulittoral macroalgae from Antarctica, the known data clearly indicate broad tolerances against the prevailing environmental, often extreme parameters.

In particular, the biochemical capability to synthesize and accumulate various protective compounds seems to be the main prerequisite for long-term survival.

The response of polar seaweeds to inorganic and organic pollutants has only randomly been investigated so far. Especially brown algae take up the radionuclide contaminant ⁹⁹Tc very strongly (Topcuoglu and Fowler 1984; Gwynn et al. 2004).

The uptake mechanisms and the actual effect of

99Tc are, however, not yet investigated. With respect to the oil spill of the Bahia Paraiso near Anvers Island, Antarctic Peninsula (Kennicutt II et al. 1990), there were no observable differences between oiled and non-oiled sites with respect to the percentage cover of either sublittoral macroalgal overstory or crustose coralline algae (Amsler et al. 1990). Similarly, Dunton et al. (1990) could not determine significant effects on photosynthesis in Porphyra endiviifoliumand Palmaria decipiens. On the other hand, Stockton (1990) reported that the principal intertidal alga, Uros- pora sp. turned brown soon after the spill. The degree of damage certainly depends on the amount and type of material released.

Seasonality of reproduction and the physiological characteristics of microscopic developmental stages

The heteromorphic life history of large brown algae is characterized by the development of

perennial sporophytes and a reduction of the gametophyte generation (Clayton 1988). The ultimate step in this evolutionary trend is observed in members of the Fucales and Asco- seirales, which lack free-living gametophytes. In Laminariales and Desmarestiales, free-living gametophytes are still present; however, they are morphologically inconspicuous, generally con- sisting of microscopic filaments and they are important mainly in sexual reproduction. It has been suggested that the dissimilar reproductive phase expression in large kelps may be primarily associated with a differential response to wave action (Neushul 1972), herbivory (Slocum 1980;

Lubchenco and Cubit 1980; Dethier 1981) or physical factors such as temperature and light (Kain 1964; Lu¨ning and Neushul 1978; Lu¨ning 1980b; Fain and Murray 1982; Novaczek 1984;

tom Dieck 1993). Early developmental stages of seaweeds (zoospores, gametophytes and small sporophytes) are shade-adapted organisms unlike the adult sporophytes (Kain 1964; Amsler and Neushul 1991; Go´mez and Wiencke 1996a; Dring et al. 1996). The different physiological performance of the heteromorphic phases has implications for algal ecology: reproduction, metabolic performance (e.g. photosynthesis) and growth are seasonally synchronized improving survival under changing environmental conditions (Lu¨ning 1990). Thus, light adaptation is an important functional character connecting the different stages of life in these species.

In Antarctic Desmarestiales reproduction and further development of gametophytes and sporophytes are governed by the photoperiod.

Culture studies carried out on all members of the Antarctic Desmarestiales indicate that life history depends strongly on the seasonal variation of daylengths. In general, the development of gametangia, fertilization (oogamy) and the formation of the early stages of sporophytes take place in winter in all Antarctic species of Desmarestiales, whereas growth of sporophytes begins with increasing daylengths in late winter-spring. In Himantothallus grandifolius, Desmarestia anceps and D. menziesii, gametophytes become fertile under short day conditions only (Wiencke 1990a;

Wiencke and Clayton 1990; Wiencke et al. 1995, 1996). InD. antarctica and Phaeurus antarcticus

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gametogenesis occurs both in short and long days.

In these species seasonality is controlled by the sporophytic stage. Sporophytes become fertile in culture at daylengths between 6 h and 8 h light per day and the developing gametophytes formed gametangia soon after germination (Clayton and Wiencke 1990; Wiencke 1990a; Wiencke et al.

1991). Similarly, in the Arctic kelp, Laminaria solidungula, sori are produced in winter (November) just before the growth of the lamina begins, but spore release does not occur until the following spring (Hooper 1984). Gametophytes become fertile in this species under short day conditions only, not under long days and short days combined with a night-break regime (Bartsch, pers. comm.). Irradiance levels < 5 lmol m^–2 s^–1 are necessary to induce gametogenesis and fertilization in Antarctic Desmarestiales (Wiencke 1990a; Wiencke and Clayton 1990; Wiencke et al.

1995, 1996). The upper temperature limit for gametogenesis is 5C in D. antarctica (Wiencke et al. 1991), a feature probably common in Desmarestiales from Antarctica.

Interestingly, all of the Antarctic Desmaresti- ales studied to date show in situ fertilization, i. e.

the juvenile sporophytes remain attached to the gametophytes (Wiencke et al. 1995, 1996). This adds new evidence for the importance of the gametophytic generation on the early stages of the large sporophytes. In terms of ecological significance, one may speculate that the recruit- ment of sporophytes and consequently the observed dominance of these species may be conditioned by the survival (or mortality) of the gametophytes.

The development of gametophytes or at least their reproductive capacity appears to be constrained by high light conditions suggesting that the fitness associated with the winter development of gametophytes lies partly in a differentiation of light requirements for photosynthesis.

For example, in Desmarestia menziesii early stages of sporophytes and gametophytes are bet- ter suited to live under low light conditions than adult sporophytes: photosynthetic efficiency (a) measured in these phases is five times higher than in adult sporophytes (Go´mez and Wiencke 1996a).

The differences in pigment allocation, cross section pathlength of radiation and general

development between the different stages account for the light harvesting efficiency at low irradiance (Ramus 1981). In filamentous or thin sheet-like thalli, pigment-based photosynthesis follows a linear curve, whereas in thick morphs, characterized by several cell layers and low ratios of photosynthetic to non-photosynthetic tissues, photosynthesis becomes uncoupled from the pigment content due to a greater self-shading (Ramus 1978).

In general, early life stages have higher dark respiration rates than adult ones, with consequences for light compensation points (Ec).

Because of their high respiration rates, Ecin gametophytes and small sporophytes are not significantly lower than in adult sporophytes, whereas the photon fluence rate required for saturation (Ek) is considerably higher in adult sporophytes due to lower a values. Photosynthesis in adult sporophytes is saturated at significantly higher irradiances (30lmol m^–2s^–1) than in gametophytes or juvenile sporophytes (16lmol m^–2 s^–1). De- spite their very high respiratory activities sporophytes and gametophytes from several Antarctic Desmarestiales show light saturation of growth at irradiances close to 10lmol m^–2s^–1 (Wiencke 1990a; Wiencke and Fischer 1990) indicating that growth is not constrained by such low irradiances (Go´mez and Wiencke 1996b).

The capacity of gametophytes and small sporophytes to grow and photosynthesize under low light conditions may be regarded as adaptive and allows the algae to survive under the seasonally changing light environment in polar regions. During winter, when incident irradiance is low and daylength is short, high photosynthetic rates and growth of gametophytes and juvenile sporophytes are favoured in virtue of their higher surface-area/volume ratio, higher pigment content and more efficient light use.

Seasonal growth and photosynthesis

In polar regions, seasons are characterized by short periods of favourable light conditions and extended periods of darkness due to polar nights and sea ice covering during winter (see chapter 2).

The seasonal development of macroalgae is